Glial fibrillary acidic protein: From intermediate filament assembly and gliosis to neurobiomarker

Trends in Neurosciences

Volumn 38, Issue 6, 2015, Pages 364-374

  Yang, Zhihui ^a   Wang, Kevin K W ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; BIOLOGICAL MARKER;

ALEXANDER DISEASE; ASTROCYTE; ASTROCYTOSIS; CELL ACTIVATION; CELL DAMAGE; CENTRAL NERVOUS SYSTEM; EXPERIMENTAL CNS INJURY; GENETIC VARIABILITY; GLIA CELL; GLIOSIS; HUMAN; INTERMEDIATE FILAMENT; INTESTINE INNERVATION; NEUROLOGIC DISEASE; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; ANIMAL; GENETICS; METABOLISM;

ANIMALS; BIOMARKERS; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HUMANS; INTERMEDIATE FILAMENTS;

EID: 84942988616     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2015.04.003     Document Type: Review

References (112)

1. Eng, L.F. et al. (2000) Glial fibrillary acidic protein: GFAP-thirty-one years (1969-2000). Neurochem. Res. 25, 1439-1451.
2. Gulbransen, B.D. and Sharkey, K.A. (2012) Novel functional roles for enteric glia in the gastrointestinal tract. Nat. Rev. Gastroenterol. Hepatol. 9, 625-632.
3. Laranjeira, C. et al. (2011) Glial cells in the mouse enteric nervous system can undergo neurogenesis in response to injury. J. Clin. Invest. 121, 3412-3424.
4. Zhang, Z. et al. (2014) Human traumatic brain injury induces autoantibody response against glial fibrillary acidic protein and its breakdown products. PLoS ONE 9, e92698.
5. Mokuno, K. et al. (1989) Neuronal modulation of Schwann cell glial fibrillary acidic protein (GFAP). J. Neurosci. Res. 23, 396-405.
6. Neuberger, T.J.T. and Cornbrooks, C.J.C. (1989) Transient modulation of Schwann cell antigens after peripheral nerve transection and subsequent regeneration. J. Neurocytol. 18, 695-710.
7. Lavoie, E.G. et al. (2011) Ectonucleotidases in the digestive system: focus on NTPDase3 localization. Am. J. Physiol. Gastrointest. Liver Physiol. 300, G608-G620.
8. Boyen and von, G.B.T. (2004) Proinflammatory cytokines increase glial fibrillary acidic protein expression in enteric glia. Gut 53, 222-228.
9. von Boyen, G.B.T. et al. (2011) Distribution of enteric glia and GDNF during gut inflammation. BMC Gastroenterol. 11, 3.
10. Clairembault, T. et al. (2014) Enteric GFAP expression and phosphorylation in Parkinson's disease. J. Neurochem. 130, 805-815.
11. Herrmann, H. and Aebi, U. (1998) Intermediate filament assembly: fibrillogenesis is driven by decisive dimer-dimer interactions. Curr. Opin. Struct. Biol. 8, 177-185.
12. Biswas, S. et al. (2011) Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert Opin. Drug Saf. 4, 433-442.
13. Rodnight, R. et al. (1997) Control of the phosphorylation of the astrocyte marker glial fibrillary acidic protein (GFAP) in the immature rat hippocampus by glutamate and calcium ions: possible key factor in astrocytic plasticity. Braz. J. Med. Biol. Res. 30, 325-338.
14. Ralton, J.E. et al. (1994) Identification of two N-terminal non-alpha-helical domain motifs important in the assembly of glial fibrillary acidic protein. J. Cell Sci. 107, 1935-1948.
15. Reeves, S.A. et al. (2005) Molecular cloning and primary structure of human glial fibrillary acidic protein. Proc. Natl. Acad. Sci. U.S.A. 86, 5178-5182.
16. Middeldorp, J. and Hol, E.M. (2011) GFAP in health and disease. Prog. Neurobiol. 93, 421-443.
17. Condorelli, D.F. et al. (1999) Structural features of the rat GFAP gene and identification of a novel alternative transcript. J. Neurosci. Res. 56, 219-228.
18. Condorelli, D.F. et al. (1999) GFAPβ mRNA expression in the normal rat brain and after neuronal injury. Neurochem. Res. 24, 709-714.
19. Nielsen, A.L. et al. (2002) A new splice variant of glial fibrillary acidic protein, GFAPε, interacts with the presenilin proteins. J. Biol. Chem. 277, 29983-29991.
20. Kamphuis, W. et al. (2012) GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS ONE 7, e42823.
21. Roelofs, R.F. et al. (2005) Adult human subventricular, subgranular, and subpial zones contain astrocytes with a specialized intermediate filament cytoskeleton. Glia 52, 289-300.
22. Choi, K-C. et al. (2009) Enhanced glial fibrillary acidic protein-delta expression in human astrocytic tumor. Neurosci. Lett. 463, 182-187.
23. Blechingberg, J. et al. (2007) Identification and characterization of GFAPκ, a novel glial fibrillary acidic protein isoform. Glia 55, 497-507.
24. Galea, E. et al. (1995) Glial fibrillary acidic protein mRNA isotypes: expression in vitro and in vivo. J. Neurosci. Res. 41, 452-461.
25. Zelenika, D. et al. (1995) A novel glial fibrillary acidic protein mRNA lacking exon 1. Brain Res. Mol. Brain Res. 30, 251-258.
26. Kamphuis, W. et al. (2014) Glial fibrillary acidic protein isoform expression in plaque related astrogliosis in Alzheimer's disease. Neurobiol. Aging 35, 492-510.
27. Hol, E.M. et al. (2003) Neuronal expression of GFAP in patients with Alzheimer pathology and identification of novel GFAP splice forms. Mol. Psychiatry 8, 786-796.
28. Boer, K. et al. (2010) Immunohistochemical characterization of the out-of frame splice variants GFAP Delta164/Deltaexon 6 in focal lesions associated with chronic epilepsy. Epilepsy Res. 90, 99-109.
29. Quinlan, R.A. et al. (2007) GFAP and its role in Alexander disease. Exp. Cell Res. 313, 2077-2087.
30. Hagemann, T.L. et al. (2006) Alexander disease-associated glial fibrillary acidic protein mutations in mice induce Rosenthal fiber formation and a white matter stress response. J. Neurosci. 26, 11162-11173.
31. Prust, M. et al. (2011) GFAP mutations, age at onset, and clinical subtypes in Alexander disease. Neurology 77, 1287-1294.
32. Yoshida, T. and Nakagawa, M. (2012) Clinical aspects and pathology of Alexander disease, and morphological and functional alteration of astrocytes induced by GFAP mutation. Neuropathology 32, 440-446.
33. Messing, A. et al. (2012) Alexander disease. J. Neurosci. 32, 5017-5023.
34. Wang, X. et al. (1997) Axonal and nonneuronal cell responses to spinal cord injury in mice lacking glial fibrillary acidic protein. Exp. Neurol. 148, 568-576.
35. Triolo, D. et al. (2006) Loss of glial fibrillary acidic protein (GFAP) impairs Schwann cell proliferation and delays nerve regeneration after damage. J. Cell Sci. 119, 3981-3993.
36. Chen, M.H. et al. (2013) Caspase cleavage of GFAP produces an assembly-compromised proteolytic fragment that promotes filament aggregation. ASN Neuro 5, 293-308.
37. Sullivan, S.M. et al. (2012) Phosphorylation of GFAP is associated with injury in the neonatal pig hypoxic-ischemic brain. Neurochem. Res. 37, 2364-2378.
38. Karl, J. et al. (2000) GFAP phosphorylation studied in digitoninpermeabilized astrocytes: standardization of conditions. Brain Res. 853, 32-40.
39. Kommers, T. et al. (1999) The mGluR stimulating GFAP phosphorylation in immature hippocampal slices has some properties of a group II receptor. Neuroreport 10, 2119-2123.
40. Inagaki, M. et al. (1994) Glial fibrillary acidic protein: dynamic property and regulation by phosphorylation. Brain Pathol. 4, 239-243.
41. Pierozan, P. et al. (2014) The phosphorylation status and cytoskeletal remodeling of striatal astrocytes treated with quinolinic acid. Exp. Cell Res. 322, 313-323.
42. Jin, Z. et al. (2013) Identification and characterization of citrullinemodified brain proteins by combining HCD and CID fragmentation. Proteomics 13, 2682-2691.
43. Romero, V. et al. (2013) Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis. Sci. Transl. Med. 5, 209ra150.
44. György, B. et al. (2006) Citrullination: a posttranslational modification in health and disease. Int. J. Biochem. Cell Biol. 38, 1662-1677.
45. Liu, D. et al. (2013) Proteomic analysis reveals differentially regulated protein acetylation in human amyotrophic lateral sclerosis spinal cord. PLoS ONE 8, e80779.
46. Oh, T.H. et al. (1995) Acidic pH rapidly increases immunoreactivity of glial fibrillary acidic protein in cultured astrocytes. Glia 13, 319-322.
47. Lee, Y.B.Y. et al. (2000) Rapid increase in immunoreactivity to GFAP in astrocytes in vitro induced by acidic pH is mediated by calcium influx and calpain I. Brain Res. 864, 220-229.
48. Fujita, K. et al. (1998) Increases in fragmented glial fibrillary acidic protein levels in the spinal cords of patients with amyotrophic lateral sclerosis. Neurochem. Res. 23, 169-174.
49. Zoltewicz, J.S. et al. (2013) Biomarkers track damage after graded injury severity in a rat model of penetrating brain injury. J. Neurotrauma 30, 1161-1169.
50. Guingab-Cagmat, J. et al. (2012) In vitro MS-based proteomic analysis and absolute quantification of neuronal-glial injury biomarkers in cell culture system. Electrophoresis 33, 3786-3797.
51. Yokobori, S. et al. (2013) Acute diagnostic biomarkers for spinal cord injury: review of the literature and preliminary research report. World Neurosurg. Published online March 19, 2013. http://dx.doi.org/10.1016/j.wneu.2013.03.012.
52. Yokobori, S. et al. (2014) Biomarkers in spinal cord injury. In Biomarkers of Brain Injury and Neurological Disorders (1st edn) (Wang, K. et al., eds), pp. 340-354, CRC Press.
53. Mouser, P.E. et al. (2006) Caspase-mediated cleavage of glial fibrillary acidic protein within degenerating astrocytes of the Alzheimer's disease brain. Am J. Pathol. 168, 936-946.
54. Tzeng, S-F. et al. (2005) Prostaglandins and cyclooxygenases in glial cells during brain inflammation. Curr. Drug Targets Inflamm. Allergy 4, 335-340.
55. Lopategui Cabezas, I. et al. (2014) The role of glial cells in Alzheimer's disease: potential therapeutic implications. Neurologia 29, 305-309.
56. Czlonkowska, A. and Kurkowska-Jastrzębska, I. (2011) Inflammation and gliosis in neurological diseases-clinical implications. J. Neuroimmunol. 231, 78-85.
57. Sofroniew, M.V. (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638-647.
58. Yu, I. et al. (2010) Glial cell-mediated deterioration and repair of the nervous system after traumatic brain injury in a rat model as assessed by positron emission tomography. J. Neurotrauma 27, 1463-1475.
59. Levison, S.W. et al. (1998) Ciliary neurotrophic factor stimulates nuclear hypertrophy and increases the GFAP content of cultured astrocytes. Brain Res. 803, 189-193.
60. Levison, S.W. et al. (1996) Acute exposure to CNTF in vivo induces multiple components of reactive gliosis. Exp. Neurol. 141, 256-268.
61. Gomes, F.C. et al. (1999) Glial fibrillary acidic protein (GFAP): modulation by growth factors and its implication in astrocyte differentiation. Braz. J. Med. Biol. Res. 32, 619-631.
62. Zamoner, A. et al. (2007) Thyroid hormones reorganize the cytoskeleton of glial cells through GFAP phosphorylation and RhoA-dependent mechanisms. Cell. Mol. Neurobiol. 27, 845-865.
63. Brahmachari, S. et al. (2006) Induction of glial fibrillary acidic protein expression in astrocytes by nitric oxide. J. Neurosci. 26, 4930-4939.
64. Tarassishin, L. et al. (2014) LPS and IL-1 differentially activate mouse and human astrocytes: role of CD14. Glia 62, 999-1013.
65. Snider, S.E. et al. (2013) Glial cell modulators attenuate methamphetamine self-administration in the rat. Eur. J. Pharmacol. 701, 124-130.
66. Kumar, A. and Loane, D.J. (2012) Neuroinflammation after traumatic brain injury: opportunities for therapeutic intervention. Brain Behav. Immun. 26, 1191-1201.
67. Johnson, K.W. et al. (2014) Ibudilast for the treatment of drug addiction and other neurological conditions. Clin. Invest. 4, 269-279.
68. Noh, H. et al. (2014) Systemic injection of LPS induces region-specific neuroinflammation and mitochondrial dysfunction in normal mouse brain. Neurochem. Int. 69, 35-40.
69. Beardsley, P.M. et al. (2010) The glial cell modulator and phosphodiesterase inhibitor, AV411 (ibudilast), attenuates primeand stress-induced methamphetamine relapse. Eur. J. Pharmacol. 637, 102-108.
70. Beurel, E. and Jope, R.S. (2009) Lipopolysaccharide-induced interleukin-6 production is controlled by glycogen synthase kinase-and STAT3 in the brain. J. Neuroinflamm. 6, 9.
71. 2+-dependent manner. J. Biol. Chem. 268, 12669-12674.
72. Frizzo, J.K. et al. (2004) S100B-mediated inhibition of the phosphorylation of GFAP is prevented by TRTK-12. Neurochem. Res. 29, 735-740.
73. Uzdensky, A. et al. (2012) Protection effect of GDNF and neurturin on photosensitized crayfish neurons and glial cells. J. Mol. Neurosci. 49, 480-490.
74. Harvey, B.K. et al. (2005) Stroke and TGF-β proteins: glial cell linederived neurotrophic factor and bone morphogenetic protein. Pharmacol. Ther. 105, 113-125.
75. Messing, A. et al. (2010) Strategies for treatment in Alexander disease. Neurotherapeutics 7, 507-515.
76. Taylor, E.M. et al. (2000) Retro-inverso prosaptide peptides retain bioactivity, are stable in vivo, and are blood-brain barrier permeable. J. Pharmacol. Exp. Ther. 295, 190-194.
77. Meyer, R.C. et al. (2013) GPR37 and GPR37L1 are receptors for the neuroprotective and glioprotective factors prosaptide and prosaposin. Proc. Natl. Acad. Sci. U.S.A. 110, 9529-9534.
78. Bargagna-Mohan, P. et al. (2007) The tumor inhibitor and antiangiogenic agent Withaferin A targets the intermediate filament protein vimentin. Chem. Biol. 14, 623-634.
79. Bargagna-Mohan, P. et al. (2010) Withaferin A targets intermediate filaments glial fibrillary acidic protein and vimentin in a model of retinal gliosis. J. Biol. Chem. 285, 7657-7669.
80. Ellis, A. et al. (2014) Systemic administration of propentofylline, ibudilast, and ( + )-naltrexone each reverses mechanical allodynia in a novel rat model of central neuropathic pain. J. Pain 15, 407-421.
81. Cho, W. et al. (2010) Drug screening to identify suppressors of GFAP expression. Hum. Mol. Genet. 19, 3169-3178.
82. Bae, M-K. et al. (2006) Aspirin-induced blockade of NF-(B activity restrains up-regulation of glial fibrillary acidic protein in human astroglial cells. Biochim. Biophys. Acta 1763, 282-289.
83. Bachetti, T. et al. (2012) Beneficial effects of curcumin on GFAP filament organization and down-regulation of GFAP expression in an in vitro model of Alexander disease. Exp. Cell Res. 318, 1844-1854.
84. Papa, L. et al. (2012) Elevated levels of serum glial fibrillary acidic protein breakdown products in mild and moderate traumatic brain injury are associated with intracranial lesions and neurosurgical intervention. Ann. Emerg. Med. 59, 471-483.
85. Okonkwo, D.O. et al. (2013) GFAP-BDP as an acute diagnostic marker in traumatic brain injury: results from the prospective transforming research and clinical knowledge in traumatic brain injury study. J. Neurotrauma 30, 1490-1497.
86. Plog, B.A. et al. (2015) Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system. J. Neurosci. 35, 518-526.
87. National Center for Injury Prevention and Control (2003) Report to Congress on Mild Traumatic Brain Injury in the United States: Steps to Prevent a Serious Public Health Problem. Atlanta, GA: Centers for Disease Control and Prevention. CDC Report, p. 45.
88. Martin, E.M. et al. (2008) Traumatic brain injuries sustained in the Afghanistan and Iraq wars. Am J. Nurs. 108, 40-47 quiz 47-48.
89. Jaffee, D.C.M.S. and Meyer, K.S. (2009) A brief overview of traumatic brain injury (TBI) and post-traumatic stress disorder (PTSD) within the Department of Defense. Clin. Neuropsychol. 23, 1291-1298.
90. Svetlov S.I. et al. (2012) Neuro-glial and Systemic Mechanisms of Pathological Responses to Primary Blast Overpressure (OP) Compared to Severe ''Composite'' Blast in Rat Models, NATO Research and Technology Organisation RTO-MP-HFM 207, 37-1-37-10.
91. Mondello, S. et al. (2012) Glial neuronal ratio: a novel index for differentiating injury type in patients with severe traumatic brain injury. J. Neurotrauma 29, 1096-1104.
92. Vos, P.E. et al. (2010) GFAP and S100B are biomarkers of traumatic brain injury: an observational cohort study. Neurology 75, 1786-1793.
93. Stein, D.M. et al. (2012) Use of serum biomarkers to predict cerebral hypoxia after severe traumatic brain injury. J. Neurotrauma 29, 1140-1149.
94. Tate, C.M. et al. (2013) Serum brain biomarker level, neurocognitive performance and self-reported symptom changes in soldiers repeatedly exposed to low-level blast: a breacher pilot study. J. Neurotrauma 30, 1620-1630.
95. Kwon, S.K. et al. (2011) Stress and traumatic brain injury: a behavioral, proteomics, and histological study. Front. Neurol. 2, 12.
96. Herrmann, M. et al. (2000) Release of glial tissue-specific proteins after acute stroke: a comparative analysis of serum concentrations of protein S-100B and glial fibrillary acidic protein. Stroke 31, 2670-2677.
97. Zhang, J. et al. (2013) Serum glial fibrillary acidic protein as a biomarker for differentiating intracerebral hemorrhage and ischemic stroke in patients with symptoms of acute stroke: a systematic review and meta-analysis. Neurol. Sci. 34, 1887-1892.
98. Wunderlich, M.T. et al. (2006) Release of glial fibrillary acidic protein is related to the neurovascular status in acute ischemic stroke. Eur. J. Neurol. 13, 1118-1123.
99. Foerch, C. et al. (2014) [Glial fibrillary acidic protein in patients with symptoms of acute stroke: diagnostic marker of cerebral hemorrhage]. Nervenarzt 85, 982-989 (in German).
100. Foerch, C. et al. (2006) Serum glial fibrillary acidic protein as a biomarker for intracerebral haemorrhage in patients with acute stroke. J. Neurol. Neurosurg. Psychiatry 77, 181-184.
101. Wagner, A.K. and Zitelli, K.T. (2013) A Rehabilomics focused perspective on molecular mechanisms underlying neurological injury, complications, and recovery after severe TBI. Pathophysiology 20, 39-48.
102. Kochanek, P.M. et al. (2011) A novel multicenter preclinical drug screening and biomarker consortium for experimental traumatic brain injury: operation brain trauma therapy. J. Trauma 71, S15-S24.
103. Zhang, Z. et al. (2010) Systems biology and theranostic approach to drug discovery and development to treat traumatic brain injury. Methods Mol. Biol. 662, 317-329.
104. O'Callaghan, J.P. and Sriram, K. (2005) Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert Opin. Drug Saf. 4, 433-442.
105. Jung, C.S. et al. (2007) Serum GFAP is a diagnostic marker for glioblastoma multiforme. Brain 130, 3336-3341.
106. Brommeland, T. et al. (2007) Serum levels of glial fibrillary acidic protein correlate to tumour volume of high-grade gliomas. Acta Neurol. Scand. 116, 380-384.
107. Moneim, I.A. et al. (1999) Autoantibodies to neurofilaments (NF), glial fibrillary acidic protein (GFAP) and myelin basic protein (MBP) in workers exposed to lead. J. Egypt. Public Health Assoc. 74, 121-138.
108. Poletaev, A.B.A. et al. (2000) Serum anti-S100b, anti-GFAP and anti-NGF autoantibodies of IgG class in healthy persons and patients with mental and neurological disorders. Autoimmunity 32, 33-38.
109. Kamchatnov, P.R. (2010) Autoantibodies to GFAP (glial fibrillary acidic protein) and to dopamine in patients with acute and chronic cerebrovascular dis@rders. Health 2, 1366-1371.
110. Ishida, K. et al. (1997) Identification and characterization of an antiglial fibrillary acidic protein antibody with a unique specificity in a demented patient with an autoimmune disorder. J. Neurol. Sci. 151, 41-48.
111. Wei, P. et al. (2013) Serum GFAP autoantibody as an ELISAdetectable glioma marker. Tumor Biol. 34, 2283-2292.
112. Zhang, Z. et al. (2009) Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways. Apoptosis 14, 1289-1298.